REVIEWARTICLE

Earthworm services for cropping systems. A review

Michel Bertrand & Sébastien Barot & Manuel Blouin &

Joann Whalen & Tatiana de Oliveira &

Jean Roger-Estrade

Accepted: 13 November 2014 /Published online: 22 January 2015# INRA and Springer-Verlag France 2015

Abstract Intensive agriculture is often criticized for negativeimpacts on environment and human health. This issue may besolved by a better management of organisms living in cropfields. Here, we review the benefits of earthworms for crops,and we present techniques to increase earthworm abundance.The major points are the following: (1) Earthworms usuallyimprove soil structural stability and soil porosity and reducerunoff. (2) Earthworms modify soil organic matter (SOM) andnutrient cycling. Specifically, earthworms stabilize SOM frac-tions within their casts, and they also increase the mineralizationof organic matter in the short term by altering physical protectionwithin aggregates and enhancing microbial activity. (3) Thepositive correlation between earthworm abundance and cropproduction is not systematic, and contrasting effects on yieldshave been observed. Earthworms induce the production ofhormone-like substances that improve plant growth and health.(4) Direct drilling increases earthworm abundance and speciesdiversity, but the beneficial effect of reduced tillage dependsupon the species present and tillage intensity. (5)Organic amend-ments enhance earthworm abundance. (6) Earthworms feeding

at soil surface are the most exposed to pesticides and otheragrochemicals. Finally, we discuss how to combinemanagementpractices, including inoculation, to increase the earthworm ser-vices. We conclude that using earthworm services in croppingsystems has potential to boost agricultural sustainability.

Keywords Earthworms . Tillage . Pesticides .

Mineralization . Belowground-aboveground interactions .

Soil structure . Crop pathogens and parasites . Ecosystemservices

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2. Effects of earthworms on soil fertility, crop growth and

health. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2.1. Earthworm activity and soil structure: consequencesfor erosion and soil water regime . . . . . . . . . . . . . . .

2.2. Effect of earthworms on soil organic matter decompo-sition and nutrients cycling . . . . . . . . . . . . . . . . . . . .

2.3. Effects of earthworms on crop growth and health . . .

3. Effects of cultural practices on earthworm communities incultivated fields . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

3.1. Tillage. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3.2. Organic amendments. . . . . . . . . . . . . . . . . . . . . . . . .3.3. Pesticides application . . . . . . . . . . . . . . . . . . . . . . . .

4.Managing earthworm beneficial effects in cropping systems5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 Introduction

Earthworms generally have positive effect on many ecosystemservices such as pedogenesis, development of soil structure,

M. Bertrand : T. de Oliveira : J. Roger-EstradeINRA, UMR, 211 Agronomie, 78850 Thiverval-Grignon, France

M. Bertrand (*) : T. de Oliveira : J. Roger-EstradeAgroParisTech, UMR 211 Agronomie, 78850 Thiverval-Grignon,Francee-mail: michel.bertrand@grignon.inra.fr

S. BarotIRD, IEES-P (IRD, CNRS, UPMC, UPEC), ENS, 46 rue d’Ulm,75230 Paris Cedex 05, France

M. BlouinUniversité Paris-Est, IEES-P (IRD, CNRS, UPMC, UPEC),61 Avenue du Général De Gaulle, 94010 Créteil, France

J. WhalenDepartment of Natural Resource Sciences, Macdonald Campus,McGill University, Ste Anne de Bellevue, QC H9X 3V9, Canada

Agron. Sustain. Dev. (2015) 35:553–567DOI 10.1007/s13593-014-0269-7

water regulation, nutrient cycling, primary production, climateregulation, pollution remediation, and cultural services (Blouinet al. 2013). They have long been used in traditional medicine(Shen 2010), due to the various chemical compounds theycontain (Grdiša et al. 2013). With a high content of proteins,about 60–70 %, they represent a valuable feed for fish (Oleleand Okonkwo 2012) or poultry (Tiroesele and Moreki 2012).They can also be a delicacy for some people, like for Ye’KuanaAmerindians in Venezuela, who eat them both raw and smoked(Paoletti et al. 2003). They attract more and more attention fortheir ability to reduce organic waste into valuable compostcalled “vermicompost” (Fig. 1). Indeed, the burial of organicwastes or their incineration is an inappropriate use of the energyand organic carbon contained within the material at a timewhen fossil energy is becoming increasingly expensive andCO2 release a major global problem. Vermicomposting oflocally produced organic wastes decreases the cost of transportto water treatment plants, incinerators, or landfills (Edwardset al. 2011). Vermicomposting represents an opportunity to turnorganic waste into a fertilizer and soil conditioner that isbeneficial for plant growth either at home, in greenhouse, oreven in the field (Arancon and Edwards 2011). These advan-tages make vermicomposting a powerful tool for environmen-tal education (Appelhof et al. 1993).

In agriculture, the beneficial effects of earthworms couldhelp to overcome some of the major issues of conventionalintensive farming (Table 1). Compaction is a major problem inhumid areas. In these cases, earthworms could help to allevi-ate structure degradation, especially if simplified tillage sys-tems are to be adopted. In conventional agriculture, with high-yield objectives, the amount of nutrients required and nitrate-leaching risk is often high. When organic amendments areapplied, earthworms could boost organic matter mineraliza-tion and improve nutrient bioavailability. Moreover, nutrientrelease due to earthworm activity is temporally and spatiallysynchronized with plant activity. Indeed, through the creationof small patches (the casts) enriched in mineral nutrients, theycould contribute to enhance nutrient use efficiency and todecrease the risks of nitrate leaching. Furthermore, reachinghigh yield levels implies a high protection level against pestsand diseases. Here again, earthworms could help: There is

evidence that earthworms help crops to be more resistant ortolerant to diseases and pests and/or could be an effectiveagent for biological control of soil pathogens. The interactionsbetween earthworms, soil functions, and plant growth and thebeneficial effects emerging from these interactions are sum-marized on Fig. 2.

However, these earthworm-mediated ecological servicesare both site- and species-dependent and may not alwaysimprove the performance of cropping systems. For instance,turnover of soil organic matter (SOM) and nutrients, acceler-ated by earthworms, could stimulate the production of green-house gases like carbon dioxide (CO2) and nitrous oxide(N2O), as shown by the meta-analysis of Lubbers et al.(2013). Nevertheless, it is generally assumed that abundantearthworm populations are beneficial to agriculture.

Since earthworms live within agroecosystems, culturalpractices exert a top-down effect on earthworm populations.Earthworm species richness, the size and structure of earth-worm populations (number of individuals, ratio of juveniles/adults), and their biomass are dependent on crop management(Riley et al. 2008; Pelosi et al. 2009). The main cultivationpractices whose influence on earthworm populations is recog-nized are summarized on Table 2. The effect of tillage onearthworm community composition and abundance is highlydependent on the intensity and scheduling of tillage opera-tions. The organic matter supplied to the soil is also a keydriver of earthworm abundance. Earthworm effects on plantgrowth or soil pathogens are expected to be highly dependenton soil properties such as SOM or water content, which arealso affected by cultural practices. Pesticides are not alwayswithout influence on earthworms. Last, the influence ofcropping systems has also to be evaluated at the territory level:Crop diversity, hedges, and land use have an influence on thespatial distribution of earthworm species. However, this as-pect will not be taken into account in this paper, due to thescarcity of studies reported in the literature.

To design crop management systems that consider thevalue of earthworms explicitly, it is necessary to assess theearthworm-mediated ecological services that occur in croppedfields and to review the effects of cultivation practices onearthworm diversity, abundance, and activity. In this paper,

Fig. 1 Vermicompost can beobtained in about 100 days fromdomestic organic wastes whenprocessed by the earthwormsEisenia fetida or Eisenia andrei.Photographs by M. Blouin

554 M. Bertrand et al.

we first review the effect of earthworms on soil fertility(including soil structure, SOM and nutrient dynamics, andmicrobial activities), plant growth, and plant health. Wethen discuss the effect of cultivation practices on earth-worm communities: tillage, organic amendments, and pes-ticide application. Finally, we discuss how earthwormscould be integrated in cropping systems to enhance agri-cultural productivity and sustainability.

2 Effects of earthworms on soil fertility, plant growth,and health

2.1 Earthworm activity and soil structure: consequencesfor erosion and soil water regimes

Soil structure is a critical factor for most soil functions, in-cluding soil fertility. Earthworms contribute to soil structure

Table 1 Lists of agriculturalissues that constrain profitablecrop production, together with theways that earthworms could helpto solve these problems

Agricultural issues Mechanisms through which earthworms can help

Deterioration of the structure of cultivated soils Earthworms improve soil aggregation and macro-porosity through their casts and galleries

Low organic matter content in cultivated soils Earthworms tend to stabilize some soil organic matterwithin their casts

Cultivated plants require large inputs of mineralnutrients and nutrient losses must be reduced

Earthworms accelerate nutrient mineralization on theshort term. Plant growth could be temporally andspatially synchronized with earthworm castingactivities, creating of small patches enriched inmineral nutrients and hormone-like effects

Pesticides use should be reduced, seek moresustainable ways to control pests and pathogens

Earthworms may decrease the negative impacts ofsome pests and pathogens (nematodes, fungi)

Fig. 2 Earthworms provide similar outcomes as cultural practices, oncrop nutrition, health and yield. The magnitude of the earthworm-inducedchanges in soil structure, water and nutrient availability, and hormone-like effects on crop health is affected by the size and activity of earthwormpopulations and other site-specific factors affecting the ability of

earthworms to modify the soil fertility and crop growth. Culturalpractices such as tillage and organic matter inputs are expected toregulate the size and activity of the earthworm community. Photographsby M. Bertrand

Earthworm services for cropping systems 555

and formation through humus formation, mineral weathering,and mixing of these components to create stable aggregates,i.e., organo-mineral complexes, which are deposited either onthe soil surface or within the soil profile (Le Bayon et al.2002). They also affect soil mechanical and hydraulic proper-ties through their burrowing activities (Fig. 3a), which gener-ate macropores that significantly impact water infiltration andthus are important for supplying crops with water, as well ascontrolling surface runoff and erosion.

Burrowing is driven by earthworm activities such as feed-ing, reaction to drought or cold temperatures, avoidance ofpredators, and soil oxygenation (Jegou et al. 2002). Poremorphology varies depending on the earthworm ecologicalgroup. Anecic earthworms (Fig. 3b) dig large (higher than 1-mm diameter) vertically oriented galleries that extend todepths greater than 1 m in the soil profile. Endogeic earth-worm (Fig. 3c) galleries are not preferentially oriented in thevertical direction. The burrow diameter is smaller than anecicburrows, and they are not so deep (Bouché 1972). Epigeicearthworms remain in the litter layer and in the first fewcentimeters of the soil and thus have little effect on soilmacroporosity. In a mesocosm experiment, Ernst et al.(2008) showed that earthworm ecological groups affect soilwater characteristics. The anecic Lumbricus terrestris and theendogeic Aporrectodea caliginosa enhanced drying in the 0–15-cm soil layer by increasing soil aeration and subsequentlyevaporation through their burrows. In contrast, the epigeicLumbricus rubellus tended to favor water storage in thetopsoil. This is probably due to the fact that L. rubellus

leaves litter at the soil surface rather than burying it, whichprevents evaporation. A. caliginosa induced higher waterinfiltration rates and faster water discharges to the subsoilthan other species, probably because its burrows aretemporary and continually being rebuilt.

Earthworm burrows affect water availability to crops.Blouin et al. (2007) showed, studying rice growing in agreenhouse, that the presence of the endogeic wormReginaldia omodeoi, formerly known as Millsonia anomala,had a positive effect on plant growth in a well-watered treat-ment, but a negative effect in a water-deficient treatment. Thiswas attributed to lower water availability to rice caused bylower soil water retention capacity in the presence of thiscompacting earthworm. However, preferential water flow oc-curred in macropores created by earthworms. This has beendocumented for different soil types: rice paddy soils (Sanderet al. 2008), temperate loamy soils (Capowiez et al. 2009), andtemperate clay soils (Jarvis et al. 2007). Preferential flowincreases the risk of leaching and subsequent contaminationof subsurface and groundwater by nitrogen and pesticides(Ritsema and Dekker 2000; Blackwell 2000). However, theaction of earthworms on soil porosity generally has a positiveeffect on the soil water regime (Ehlers 1975; Clements et al.1991; Pitkänen and Nuutinen 1998). Clements et al. (1991)showed that, after 10 years of earthworm inoculation, thewater infiltration rate increased from 15 to 27 mm h−1. InMediterranean soils, water percolation was found to be posi-tively correlated with earthworm biomass, burrow length, andburrow surface with r value of 0.66, 0.65, and 0.77,

Table 2 Challenges to maintainlarge, active populations ofearthworms in agroecosystemsand possible solutions

Effects of cultivation operations in conventionalagriculture

Changes in cultivation practices beneficial toearthworms

Tillage tends to reduce earthworm populations,especially anecics.

No-tillage or reduced tillage

Some pesticides impact earthworm populationsnegatively

Reduced use of pesticides; alternative ways tocontrol pests and pathogens

In conventional agriculture, organic amendments arescarce and litter availability is reduced.

Increase soil organic matter supply; reducetillage;introduce cover crops; agro-forestry.

Simplification of crop sequence, elimination ofecological infrastructures (hedges, woods,…).

Diversification of the crop sequence, introduction ofpermanent pastures, (re)conception of ecologicalinfrastructure.

a) b) C)

Fig. 3 a Earthworm gallery in a compacted clod of loamy soil in Northern France (credit C. Pelosi). bAnecic earthworm Lumbricus terrestris (credit S.Barot). c Endogeic earthworm Apporectodea rosea (credit C. Pelosi)

556 M. Bertrand et al.

respectively (Bouché and Al-Addan 1997). In this study, asignificant correlation between infiltration and earthwormbiomass was observed: The infiltration rate increased by150 mm h−1 per 100 g m−2 of earthworms. This correlationwas even stronger when only anecic species were consideredin the analysis: 282 mm h−1 per 100 g of anecic m−2 (Bouchéand Al-Addan 1997). In contrast, in a corn agroecosystemwhere earthworm populations were deliberately elevated, theinfiltration rate did not vary (Lachnicht et al. 1997).

Water infiltrating through earthworm burrows can be asource of crop water or percolate through the soil profile, butchanges in water infiltration also affect surface hydrologicalprocesses. In Ohio, the increase in infiltration rate due toanecic earthworm burrows reduced soil erosion by 50 %(Shuster et al. 2002). In Vietnam on an experimental fieldwith 40 % slope, biogenic aggregates of Amynthas khamiwere responsible for a 75 % decrease in runoff (Jouquetet al. 2007). Endogeic species also increase soil macroporosityand water infiltration, which tends to reduce runoff. However,it has been shown that some endogeic species also producesmall-sized casts, which favor surface sealing and contributeto soil erosion (Blanchart et al. 1999). This effect was shownin tropical conditions with Pontoscolex corethrurus, a tropicalearthworm. However, this negative effect resulted from adramatic population increase of one particular species afterthe land use was changed from forest to pasture in Brazil(Chauvel et al. 1999). Earthworm species that create waterstable casts reduce soil sensitivity to splash effects and runoff,but this may reduce water infiltration by increasing surfacebulk density (Reddell and Spain 1991b; Blanchart et al. 1999;Chauvel et al. 1999; Shuster et al. 2002). These contradictionsbetween the results about the impact of earthworms on soilstructure, water infiltration, and soil erosion are probably dueto the fact that this impact depends on the following: (1) therainfall regime, (2) earthworm abundance, (3) earthwormspecies, and (4) the amount of organic matter available at soilsurface (Blanchart et al. 1997; Hallaire et al. 2000).

Generally, earthworm burrowing and casting activities con-tribute efficiently to soil erosion control in temperate andtropical soils. In temperate climates, anecic earthworm castsincreased soil roughness, reinforced by the presence of organ-ic residues, forming “middens” that reduced surface runoff(Le Bayon et al. 2002). In Finland, surface runoff duringrainfall events was negatively correlated with the dry biomassof L. terrestris (Pitkänen and Nuutinen 1998). In three soiltillage treatments where earthworm populations were reduced,increased, or remained unmanipulated, anecic earthworm bio-mass was identified as an important independent variablecontributing to runoff and erosion diminution, and erosionrates decreased exponentially as a function of anecic earth-worm biomass (Valckx et al. 2010). Endogeic and anecic castson the soil surface improve soil structural stability and give abetter resistance to erosion (Le Bayon et al. 2002). They may

represent considerable amounts of soil, i.e., 2 to 10 kg m−2 intemperate climate, which corresponds to a 5- to 25-mm-thicklayer created by earthworms.

Although some cases of soil degradation due to earthwormcompacting species are reported in the literature, earthwormsgenerally improve soil structural stability and soil porosity andreduce runoff.

2.2 Effect of earthworms on soil organic matter and nutrientcycling

Earthworms contribute to carbon cycling through severalcomplementary mechanisms (Lavelle and Martin 1992;Marinissen and de Ruiter 1993). Anecic and epigeic earth-worms directly ingest poorly decomposed litter at the soilsurface, while endogeics ingest soil and assimilate a smallfraction of the organic matter it contains. Once ingested, thefraction of litter that is not assimilated is fragmented duringthe digestion process and mixed with soil. Last, the undigestedlitter and SOM are returned to the soil in the form of earth-worm casts. Fresh casts possess active bacteria and highmineralization rates, at least transiently, and these nutrientcycling processes decline with the age of casts.

SOM decomposition and mineralization depend on pro-cesses mediated by soil microorganisms. Earthworms changethe structure of soil microbial communities in a way thataccelerates SOM decomposition and mineralization (see forexample Scheu et al. 2002; McLean and Parkinson 2000).Bacteria are strongly implicated in soil organic carbon (SOC)stabilization and nitrogen cycling due to their population size,turnover rates, and ability to produce enzymes required fordecomposition/mineralization. While bacteria directlycontribute to SOM mineralization, Winding et al. (1997)observed greater protozoa activity in mesocosms with earth-worms, which increased mineralization, presumably due topredation of bacteria in the detrivorous food web. Four mech-anisms are generally assumed to be responsible forearthworm-microbial interactions (Brown 1995): (i) Soil in-gestion stimulates the growth of some microorganismsthrough the addition of mucus and brings microorganisms incontact with organic residues. (ii) The incorporation of organ-ic matter into the soil creates hot spots of microbial activity.(iii) Earthworms modify soil structure, creating habitats favor-able to microbial activity. (iv) Earthworms are responsible forhorizontal and vertical transport of microorganisms, which areeither transported on earthworm body or in their gut, ingestedwith soil or litter. While the stimulation of some bacteriawithin the earthworm digestive tract and in fresh casts is oftenreported, the long-term effect of earthworms on bacteria bio-mass in the bulk soil is still under debate. In some studies,bacterial biomass increased in response to earthworm stimu-lation (Burtelow et al. 1998; Li et al. 2002; Groffman et al.

Earthworm services for cropping systems 557

2004) and decreased following earthworm consumption inother studies (Hendrix et al. 1998; Groffman et al. 2004).

The short-term increase in mineral nutrient availability inthe presence of earthworms is well documented, but the long-term effect of earthworms on SOM content is less clear(Lavelle et al. 1992; Don et al. 2008). Incorporation of organicmatter into the soil profile by earthworms might lead to apartial protection of surface litter within the SOM. The evi-dence for this phenomenon comes first from the lower miner-alization observed in old and stable earthworm casts(Pulleman et al. 2005; Bossuyt et al. 2005). Second, theorganic matter that reaches a deeper soil layer is less proneto decomposition, which might be due to the lower provisionof fresh organic matter to these soil layers that suppressespositive priming effects (Fontaine et al. 2007), i.e., the en-hancement of SOM decomposition through inputs of labileorganic matter that stimulates microbial activities.

Bohlen et al. (1997) calculated that a population of about100 individuals per m2 of L. terrestris could ingest840 kg ha−1 year−1 of surface litter in a temperate cornfield.Eriksen-Hamel andWhalen (2007) reported that the availabil-ity of soil mineral N, and subsequently the N concentration insoybean grain, is increased with the abundance of earth-worms, mostly A. caliginosa. The increase in N availabilitywith increasing earthworm abundances can be significant: Afield with high earthworm abundance, 300 individuals m−2,could have 14 kg N ha−1 more in the 0–15-cm soillayer than a field with low earthworm abundance, 30individuals m−2. The availability of some of the water-soluble nutrients (K, Ca, Mg,…) is also enhanced asSOM and litter pass through earthworm gut, because thesenutrients are solubilized and dissolved from soil mineralsduring the grinding/rearrangement of organo-minerals duringgut transit (Carpenter et al. 2007).

Earthworms may also cause N losses from ecosystems. Forexample, earthworms have been shown, in some cases, toincrease denitrification (Horn et al. 2006; Costello andLamberti 2009; Lubbers et al. 2013) and the leaching ofmineral N (Domínguez et al. 2004). However, the stabilizationof organic N in earthworm casts could offset these N losses.Such effects of earthworms on the nitrogen balance have notbeen assessed thoroughly in agroecosystems, and this knowl-edge gap needs to be addressed.

In summary, processes underlying earthworm’s effects onSOM cycling and nutrient availability are complex, and thebalance between positive and negative effects is not clearlyestablished and probably depends on the time of sampling at aspecific site.

2.3 Effects of earthworms on crop growth and health

Earthworms have inhabited soils for several hundred millionyears and represent the most abundant belowground biomass

in most terrestrial ecosystems (Lavelle and Spain 2001); so, itis likely that coevolution between earthworms and plantscould have occurred. The beneficial effect of earthworms onplant growth was recognizedmore than a century ago (Darwin1881). Consequently, the effect of earthworms on primaryproduction has been extensively investigated in the laboratoryor in the field, respectively, 46 and 54 % of the studiesreviewed by Brown et al. (1999), with some experimentsmonitored for several years (Giri 1995; Blanchart et al.1997). Here, we give a brief overview of some of the vastliterature available on this topic (Lee 1985; Edwards andBohlen 1996; Lavelle et al. 2001; Edwards 2004).

Brown et al. (1999; 2004) reviewed 246 experiments intropical countries and concluded that in 53 % of the studies,there was less than 20 % difference in biomass productionwith and without earthworms. In 4 % of studies, there wasmore than 20 % reduction in biomass production in thepresence of earthworms, such that earthworms were detrimen-tal to plant growth. In the remaining 43% of studies, there wasmore than 20 % improvement in biomass production whereearthworms enhanced plant growth. Several environmentalfactors were identified as responsible for variation in biomassproduction in the presence of earthworms (Brown et al. 1999,2004). A major determinant is soil type, especially soil textureand carbon content, which account for 43% of the variation inplant yield response. Sandy soils with a slightly acidic pHshow the greatest increase in biomass production in the pres-ence of earthworms (Brown et al. 2004), which was confirmedby Laossi et al. (2010a). Plant functional group is also animportant driver: Earthworms induce higher biomass produc-tion in perennial species, especially trees, than that in annualspecies, whereas biomass of legumes is sometimes negativelyaffected by the presence of earthworms (Brown et al. 2004).

In a review of 67 studies reporting 83 cases located intemperate countries, Scheu (2003) showed that abovegroundproduction increased significantly with earthworms in 79% ofcases, while it decreased significantly in 9 % of cases.Belowground production increased significantly in 50 %of cases and decreased in 38 % of cases. The shoot-rootratio was assessed in 24 % of cases and increased withearthworm abundance in all cases but one study reportedby Atiyeh et al. (2000). To summarize, aboveground bio-mass generally increases in the presence of earthworms,but belowground biomass exhibits a variable response tothe presence of earthworms.

The positive correlation between earthworm abundanceand crop production is not systematic, and contrastingeffects on yields have been observed. For example, a studyby Baker et al. (1999) showed that pasture production in-creased linearly with increasing earthworm abundance,A. caliginosa, Aporrectodea longa, and Aporrectodeatrapezoides, being each introduced at 114, 214, 429, and643 earthworms per m−2. Conversely, Chan et al. (2004)

558 M. Bertrand et al.

reported that the highest grass production, +49 % higher thanthat in control without earthworms, was measured in the lowabundance treatment, 212 A. longa per m2, not in the highabundance treatment, 424 worms per m−2. This negative effectof high earthworm abundance on crop production is not fullyunderstood, but it could be that adding earthworms above thesoil carrying capacity will lead to soil compaction, as observedin Amazonia (Chauvel et al. 1999).

Five mechanisms, reviewed in Brown et al. (2004), arelikely responsible for the positive effect of earthworms onplant production. Earthworm-induced changes in soil physi-cochemical properties, reviewed in Sect. 1, include the fol-lowing: (i) modification of soil porosity and aggregation,which changes water and oxygen availability to plants, and(ii) greater mineralization of SOM, which increases nutrientavailability to the plants. The other three mechanisms involveinteractions with other organisms: (iii) biocontrol of pests andparasites, (iv) stimulation of symbionts, and (v) production ofplant growth regulators via the stimulation of microbialactivity.

Earthworms could be effective for pest biocontrol. Forexample, earthworms Aporrectodea rosea and A. trapezoidesreduced the severity of take all, due to a soil-borne fungalpathogen (Stephens et al. 1994; Stephens and Davoren 1997),and the earthworm R. omodeoi reduced the damage caused byplant parasitic nematodes Heterodera sacchari on rain-fedrice plants (Blouin et al. 2005). Earthworms influenced thedevelopment of aphids through their effects on plant growthand nutrient content (Scheu et al. 1999; Eisenhauer andScheu 2008). While the increase in nutrient availability inthe presence of earthworms could increase plant resistanceagainst herbivores, this effect has never been demonstratedin the field. Another way that earthworms could benefitagricultural crop production would be to control weeds,which is possible through their ability to modify seed ger-mination by burial, ingestion, and maternal effects (Laossiet al. 2010b). This idea is supported by the influence ofearthworms on natural plant community structure, which canincrease or decrease plant density depending on the plantand earthworm species (Decaëns et al. 2003; Hale et al.2008; Laossi et al. 2009; Eisenhauer et al. 2009), but needsto be confirmed in agroecosystems to determine whether areduction in herbicide use is possible when earthworms areabundant.

Earthworm interactions with other soil organisms havereceived less investigation. For instance, the spreading ofsymbionts, i.e., mycorrhizae, carried by earthworms colo-nizing new fields was shown by Gange (1993), andDoube et al. (1994) demonstrated that earthworms canincrease the nodulation of legume plants by Rhizobium.However, to our knowledge, crop production in responseto an earthworm-enhanced redistribution of mycorrhizae orRhizobium has never been assessed.

Greater production of plant growth regulators in the pres-ence of earthworms was demonstrated (Canellas et al. 2002;Muscolo et al. 1998). These compounds could includesignal molecules such as auxin or ethylene produced inearthworm casts, as demonstrated with loss-of-functionmutants of Arabidopsis thaliana and transcriptome analysisof earthworm effects on plant development and defense(Puga-Freitas et al. 2012a). The stimulation of cultivablebacteria producing indoleacetic acid, an auxin compound,was also demonstrated (Puga-Freitas et al. 2012b).

Most of these findings regarding effects of earthworms onplant growth and health are positive but tend to be fromstudies under controlled conditions. Due to the great numberof processes involved and the variability of field conditions,it is difficult to confirm these effects in agroecosystems,indicating that more research is needed on earthworm-plantinteractions in real environments.

3 Effects of cultural practices on earthworm communitiesin cropped fields

Cultural practices are widely recognized to affect earthwormsin agricultural fields (Lee 1985; Edwards and Bohlen 1996;Chan 2001; Roger-Estrade et al. 2010). Several studies haveshown that earthworm abundance and diversity are reduced inagricultural fields, compared to uncropped soils (Edwards andBohlen 1996; Peigne et al. 2009). Moreover, earthworms aremore abundant in permanent pastures than those in annuallycropped agroecosystems (Low 1972). The cultural practicesmost often cited for their effects on earthworm populations aretillage, crop sequence, organic fertilizers, and pesticide use,discussed further in the following sections.

3.1 Tillage

It is well known that tillage affects earthworm communitystructure and population dynamics. Tillage intensity, whichcan be defined as a combination of (i) working depth, (ii)fragmentation mode, and (iii) frequency of operations, is amajor controller of earthworm population size and diversity.The working depth could be superficial, to a depth of 5–10 cmin a shallowly harrowed soil, or extensive in soils that aresubject to full-inversion plowing (to a depth of 15–20 cm) andsubsoiling (below 20-cm depth) operations. Fragmentation ofsurface litter is greater in soils that are rototilled than withsome conservation tillage equipment (e.g., chisel plow withsweeps) or shallow harrows (e.g., chain harrow used forburying seed). The frequency of operations could be high,especially in organic farming (OF) systems where tillage iswidely used to control weeds. Ivask et al. (2007) showed thatearthworm populations are sensitive to tillage frequency.

Earthworm services for cropping systems 559

Earthworms are affected by tillage through several mecha-nisms (Chan 2001; Curry 2004; Roger-Estrade et al. 2010).The main, direct impact is the mechanical damage of earth-worms that causes physical injuries or death following contactwith tillage tools or soil clods moved during the tillage(Gerard and Hay 1979). Boström (1995) estimated that 61 to68 % of the earthworm biomass present in the soil layer tilledby a rotary hoe was killed by the tool. Soil inversion byplowing exposes earthworms to predators by moving deep-dwelling earthworms to the soil surface (Cuendet 1983;Tomlin and Miller 1988) and also causes desiccation or frostdamage to cocoons when tillage operations occur in autumnafter crop harvest (House and Parmelee 1985). Conventionaltillage (plowing and secondary tillage operations) destroysearthworm burrows, removes the insulating layer of litter,modifies organic matter availability due to burial of cropresidues (Lee 1985; Nuutinen 1992; Briones and Bol 2003),and changes soil physical conditions such as temperature,moisture, and soil structure (Birkas et al. 2004; Rosas-Medina et al. 2010). Soil compaction, which can occur whenwet soils are cultivated, has a detrimental effect on earthwormcommunities, inducing earthworm avoidance of compactedzones and earthworm death due to crushing by machinery(Capowiez et al. 2009; Cluzeau et al. 1992; Larink andSchrader 2000).

The less intensively the soil is disturbed, the less harmfultillage is for the earthworms. Thus, superficial tillage was lessharmful for earthworms than ploughing. The impact ofploughing on earthworms was reviewed extensively(Edwards and Bohlen 1996; Chan 2001; Kladivko 2001).Even if ploughing is generally detrimental to earthworms,results vary across agroecosystems. After 5 years of cultiva-tion with ploughing, there was a decrease of approximately70 % in earthworm biomass and 80 % in earthworm numbers(Chan 2001). However, Evans and Guild (1948) foundthat a single spring ploughing did not significantly reducethe biomass or total number of earthworms. Rosas-Medinaet al. (2010) found no difference between shallow tillage,disk ploughing, and ripper decompaction on earthwormabundance and biomass. Pelosi et al. (2009) found threeto seven times more anecic and epigeic earthworms in adirect seeded system with living mulch treatment thanthose in conventional or organic farming systems withploughing, and there were approximately two times moreendogeic earthworms in conventional and organic farmingploughed systems than those in the direct seeded system.

As indicated by the findings of Pelosi et al. (2009), earth-worm ecological groups respond differently to soil tillage(Ivask et al. 2007; Capowiez et al. 2009). Epigeic earthwormsare negatively impacted by ploughing, as they cannot accessto their trophic resource after burial of crop residues into thesoil. The anecic group is probably the most negatively im-pacted by soil tillage because anecic species tend to be large,

which makes them vulnerable to mechanical damage. Theirvertical burrows are permanent and used as shelters—in con-trast to the temporary burrows of endogeic species—as well asan access route to crop litter (their main food source) at the soilsurface. Destruction of anecic burrows by tillage likely has anegatively impact on anecic earthworms. Peigne et al. (2009)explained that the increase in earthworm abundance in theirno-till treatment was due to greater numbers of anecics.Endogeic earthworms seem to be less impacted, and evensometimes favored by ploughing, as their access to organicmatter is facilitated when crop residues are buried and partiallydecomposed by soil microorganisms (Nuutinen 1992; Wyssand Glasstetter 1992). The endogeic earthworm A. caliginosawas considered to be tolerant of soil tillage (Peigne et al. 2009;Rosas-Medina et al. 2010) although de Oliveira et al. (2012)found it to be more sensitive to tillage than A. rosea. Pelosiet al. (2009) estimated that endogeic earthworms represented75 % of total earthworm populations in ploughed fields (con-ventional and organic farming systems) and only 36 % inunploughed ones (direct seeded system). We suggest thatcontrasting response of earthworm populations to tillage inthese field studies is due to the variability in the abundanceand structure of earthworm populations during the year andbetween years. Thus, in field studies, the choice of the sam-pling date is crucial. A given tillage operation probably has adifferent effect on a population with a high proportion ofjuveniles than that on a population dominated by aged adultsbecause juveniles may be more susceptible to mechanicaldamage and lack of food availability than adults. Moreover,the sensitivity of the different stages likely depends on theearthworm species. Thus, better description of the impact oftillage on earthworm communities requires monitoringthroughout the year and for several years in adjacentagroecosystems with no-till and tillage treatments. These datacould calibrate population dynamics models, to have an ideaof the earthworm dynamics in undisturbed soils and finallyanalyze the effect of tillage practices on earthworm populationdynamics.

Therefore, farmers who want to protect (or enhance) earth-worm diversity and abundance in their fields have to carefullychoose the tillage system they use (a light harrow for instanceis better than a more aggressive rototiller for secondary till-age), the scheduling (prefer tillage in winter than in spring,because at that period, the population is dominated by juvenilethat are more sensitive to tillage than adults), and the intensity(prefer unploughed than ploughed systems whenever possi-ble). Direct drilling with direct seeding/no-till equipment isthe most earthworm-friendly tillage practice. However, thistype of crop management often poses challenges for weedcontrol. Innovative approaches for the application of conser-vation tillage, such as perennial mulches, mechanical controlof cover crops, rotational tillage, and others still need to beassessed for their impact on earthworms (Peigné et al. 2007).

560 M. Bertrand et al.

3.2 Organic amendments

Applying organic matter to agroecosystems is favorable toearthworm communities (increasing abundance and/or speciesdiversity), regardless of the product applied (crop residue,green waste, cattle manure, etc.), since dead organic matteris the food of earthworms. However, the extent to whichearthworm populations and species diversity increases de-pends on the amount and quality of organic amendmentsapplied to the soil and the feeding habits of earthworm species(described above, for the epigeic, endogeic, and anecic eco-logical groups).

The quality of crop residues and organic amendmentsapplied to the soil influences the humus content and conse-quently benefits endogeic earthworms that feed on humidifiedorganic matter. Since the humification process is, amongother things, controlled by the carbon to nitrogen ratio ofthe residues, the biochemical composition of residuescould be considered as a qualitative indicator of the foodresources supplied to endogeic earthworms. Thus, the cropsequence (including cover crops) is important to consider,because it determines the biochemical composition of theorganic matter entering the agroecosystem.

Many agricultural systems have integrated cropping andlivestock production, which is a source of animal manure(often from cattle) that serves as food for earthworms.Dung from various herbivores as an organic substrate forearthworm populations was reported by Scown and Baker(2006). These authors found that horse dung was generallypreferred by five earthworm species (A. trapezoides,Microscolex dubius, M. phosphoreus, Spenceriella macleayi,and S. bywongensis). Leroy et al. (2008) compared farmyardmanure, cattle slurry, and various composts on field earth-worm populations. Two and a half years after the first organicmatter application, the farmyard manure and cattle slurrytreatments had the largest number of earthworms (about800–900 individuals m−2), while the unamended controlshad the lowest earthworm abundance (about 150 individualsm−2). The three compost treatments had intermediate values(400–500 individuals m−2).

Due to the paucity of data describing the response of fieldearthworm populations to quantity or quality of organicamendments originating from crop residues and other sources,it is not clear how to designing farming systems with appro-priate organic matter inputs to maximize earthworm abun-dance and diversity.

3.3 Pesticide application

Most data about pesticide effect on earthworms come fromstandard laboratory tests with the epigeic Eisenia fetida, acompost-dwelling earthworm that is absent from agriculturalfields. Due to the distinct life cycle and ecological niche of

E. fetida, it is challenging to determine how normal field-dwelling earthworms will respond to pesticides (Pelosi et al.2014). The pathways and duration of exposure to potentiallytoxic compounds in pesticides (active compounds and adju-vants) need to be considered for field-dwelling earthworms.

Fungicides and insecticides are reported to be directly toxicto earthworms (Pelosi et al. 2014). However, they are fre-quently sprayed on foliage of crops after canopy closure, sothat earthworms are not directly in contact with these pesti-cides and do not ingest them; unless, it rains shortly afterspraying (washing pesticides off the foliage, bringing theminto the soil), or if contaminated leaves fall onto the soil.Copper-based fungicides, common in organic farming, canbe toxic to earthworms. In South Africa, Eijsackers et al.(2005) studied the direct toxic action of copper oxychlorideon earthworms in vineyards and showed that copper couldaccumulate in earthworm. This element reduced growth andsurvival and induced behaviors such as a low burrowing rateand avoidance of copper-contaminated soils. Molluscicidesmay endanger anecic earthworm populations if the applicationis followed by a rainy period that causes anecic earthworms tomove to the surface, where they may ingest the product.Vermifuges used for cattle care are excreted in dung, wherethe vermifuge products or their derivatives can be ingested byearthworms, although Svendsen et al. (2005) reported limitedimpact of vermifuges on the life cycle of earthworms.Herbicides from various chemical families have a wide rangeof toxicity for earthworms. For instance, Mohasin et al. (2005)have showed that paraquat applied at commercial dose in-duced a stronger decrease in cast formation, compared to acontrol plot without herbicide application, than glyphosatealso applied at commercial dose. Herbicide applications aremade on the soil surface, prior to planting or following weedand crop emergence, so that epigeic and anecic earthwormsthat feed on surface litter may be impacted by herbicides.

Exposure pathways differ for each type of pesticide and canbe coupled with information on earthworm habitat and feed-ing preferences to draw some general conclusions about howpesticides affect earthworms. Endogeic earthworms are notdirectly exposed to pesticides sprayed on crop foliage or onthe soil surface, and they do not feed on fresh organic matterthat may contain pesticide residues. Therefore, their exposureto pesticides is expected to be low. Epigeic earthworms are themost exposed to agrochemicals, as they live and feed at thesoil surface. Anecic earthworms are also exposed to pesticidesas they feed on plant litter found on the soil surface. Pesticideimpacts on earthworm communities are expected to be greaterin no-till than tilled agroecosystems for two reasons: (i)Endogeic species dominate earthworm communities in conven-tionally tilled fields, and their life history traits reduce theirexposure to pesticides, and (ii) no-till fields have greater relianceon herbicides for weed control, and this is likely to increaseexposure to pesticides of epigeic and anecic earthworms, which

Earthworm services for cropping systems 561

represent the larger proportion of the earthworm communities inno-till agroecosystems.

Toxicity of pesticides to earthworms is difficult to assessfrom laboratory experiments because effective pesticide ap-plication rates in the field are generally low compared to toxiclevels used in laboratory experiments. Under field conditions,lethal effects are rarely observed when the products are used atnormal application rates, but sublethal effects on growth andreproduction may occur, depending on the earthworm speciesand product used (Bauer and Römbke 1997). For example,Choo and Baker (1998) reported no significant reduction ofgrowth after 5 weeks of exposure to endosulfan (insecticide)and fenamiphos (used as an insecticide and a nematicide) but asignificant growth reduction with ridomil (fungicide) andmethiocarb (used as bird repellent, insecticide, acaricide, andmolluscicide).

Therefore, the conclusion that can be drawn from availableliterature is that most data on pesticide toxicity to earthwormsis based on E. fetida response in standard tests with well-fedearthworms having optimal population density. A more real-istic assessment of ecotoxicological risk to pesticides requiresinformation that better reflects the potential exposure in thefield, with typical pesticide application rates and consideringearthworm population dynamics in response to fluctuatingenvironmental conditions (Menezes-Oliveira et al. 2011).

4Managing earthwormbeneficial effects in cropped fields

Increasing biodiversity in cropping systems is the key toimprove agriculture sustainability, and diverse earthwormcommunities can contribute positively to this objective(Brussaard et al. 2007; Malezieux 2012). Depending onfarmers’ objectives, there are a variety of strategies to promoteearthworm populations and earthworm services for agricultur-al crops. As illustrated in Fig. 4, these strategies range fromthose requiring minimal human intervention (self-organizedecosystems) to those that require considerable human inter-vention, including the use of earthworm-engineered products.

The first way to maintain large earthworm populations isby adopting practices that conserve earthworms or allow themto recolonize fields. Earthworm communities withinagroecosystems can be considered to function as meta-communities (Mouquet and Loreau 2003), meaning that theirabundance and diversity vary with land use (e.g., permanentpastures generally host larger earthworm populations thanwheat fields). Managing earthworms across the landscapecontext implies that land owners should retain enough patchesof land with earthworm-friendly land uses to serve as sourcesof earthworms (i.e., spatially control earthworm populations).Temporally, farmers can select crop rotations that includephases with earthworm-friendly crops/land uses to increase

depleted earthworm populations. To achieve these objectives,it is necessary to modify the cropping systems at the farmscale or landscape scale to introduce cultural practices that arebeneficial for earthworms and avoid practices that are detri-mental to earthworms. Still, these practices must sustain cropproduction and allow farmers to meet crop yield targets. Forinstance, reduction in tillage intensity is favorable to earth-worms, but, if adopted, alternative weed control measures areneeded, e.g., using cover crops and/or livingmulches, to avoidyield losses. Other practices that are beneficial to both earth-worms and crops could represent win-win strategies. Forinstance, increasing the organic matter inputs to the soil orliming to bring the pH to a level favorable to earthworms andcrops. These actions not only promote earthworm populationsbut could be the beginning of a virtuous circle: Adding organ-ic matter or buffering soil pH promotes earthworm density butalso improves soil structure and SOM cycling through bene-ficial earthworm-microbial interactions. In turn, greater soilbiological activity can positively stimulate crop growth, lead-ing to greater organic matter inputs from crop residues. Thispoint is particularly important because agricultural activitiestend to decrease SOM worldwide (Lal 2004).

The second way to increase earthworm abundance is toinoculate them directly into the field. However, this relies onthe existence of an earthworm production unit or a commer-cial source of earthworms. Earthworms can be introducedwithout organic matter, but there should be enough organicmatter in the field to meet the feeding requirements of theintroduced and indigenous (if any) earthworm populations.Adding organic matter with earthworms is possible, but or-ganic matter has then to be retrieved from outside the field,which makes the technique dependent on the cultural systemand/or the socioeconomical context.

From laboratory breeding, it seems that the developmentstage of the introduced earthworms must be considered, ascocoons and juveniles are more adaptable to the transfer fromone soil to another than adults. Earthworm inoculation units(Butt et al. 1997) are plastic bags containing the three earth-worm life stages (cocoons, juveniles, and adults) that areemptied in field holes. This technique increases the successof colonization, as it involves addition of a structured popula-tion. The Stockdill method (Stockdill 1959, 1966, 1982;Martin and Stockdill 1976) is based on transplanting soilblocks with earthworms from adjacent ecosystems to theagroecosystem. This method aims to introduce earthwormsfrom all life stages within an intact matrix of soil and associ-ated organisms. However, this technique can be damaging forthe ecosystem where soil blocks are retrieved.

At the other end of the gradient (Fig. 2), services provided byearthworm populations can be accessed by using productsengineered by earthworms in semi-industrial production sys-tems. Spreading of earthworm-created products, such asvermicompost, enters this category. Vermicompost, amesophilic

562 M. Bertrand et al.

compost made by earthworms, is produced from organic wastes;so, this solution could be very efficient for farmers with live-stock operations as well as field crop cultivation. In fact, animalwastes could be vermicomposted at the farm, generally using theearthworm species E. fetida, and then spread with a minimaltransport cost. The use of vermicompost extracts is also possible,but the cost associatedwith extraction prohibits their use in field-scale agriculture. However, they can be used in plant nurseries tofortify young seedlings (Edwards et al. 2011).

Despite all these techniques, there are few long-term fieldexperiments examining earthworm impacts on soil fertilityand crop yield, partially because it is difficult to controlearthworm abundance in large plots so that high and lowearthworm abundances could be compared among agriculturaltreatments (e.g., to evaluate the effects of tillage, organicmatter amendments, mineral fertilizer, pesticides). Therefore,despite many indirect arguments and results demonstrating thebeneficial effect of earthworms on crop growth and yield theshort term, it is difficult to scientifically assess the long-termbenefits of increasing earthworm abundance in cropped fields.

In the same vein, all components of agroecosystems inter-act, and the choice of the plant is probably important fordetermining earthworm-crop interactions. For example, somecrops are probably more beneficial for earthworms becausethey produce more crop residues (e.g., higher root biomass) orlead to the accumulation of SOM stocks that can serve as foodfor earthworms. For the same reason, different cultivars of thesame crop plant are likely to impact earthworms differently,but how cultivar traits impact earthworms has hardly beenstudied. Reciprocally, earthworms are likely to affect differ-ently diverse plant cultivars. For instance, rice cultivars re-spond differently to the presence of earthworms (Nogueraet al. 2011). This suggests that choosing the right cultivar ordeveloping new cultivars that interact well with earthwormscould amplify the benefit of earthworm-friendly croppingsystems. Modern cultivars were developed principally for

their high yields and quick growth, and no effort was madeto select cultivars that interact fruitfully with soil biodiversity(Loeuille et al. 2013). This represents an important researchavenue to promote soil biodiversity for better crop productionin the context of sustainable agriculture.

Due to the inadequate number of long-term field experi-ments on earthworms, the site-specific nature of earthwormservices to crops and the absence of socioeconomic evaluationof techniques to increase earthworm numbers, the promotionof earthworm in agricultural fields is still anecdotal. However,increasing knowledge about their contribution to soil func-tioning and about the ecosystem services they provide isstimulating enthusiasm for earthworm experiments by farmersand researchers. This growing interest will probably fillknowledge gaps and provide socioeconomic informationregarding the opportunity to promote earthworms incropping systems. In any case, earthworms are key actorsin soil biodiversity, and they will likely be important inthe development of innovative, sustainable cropping sys-tems in the foreseeable future.

5 Conclusion

Overall, earthworm effects on soil fertility and plant growthare positive. They improve soil structure and stabilize SOMfractions within their casts. In the short term, they increasemineralization, which make mineral nutrients available forplants. Earthworm trigger the release of molecules analoguousto phytohormones that tend to improve plant growth. Tillageis generally detrimental to earthworms whereas practices in-creasing SOM content positively impact earthworm commu-nities. The impact of pesticide of earthworms is incompletelyunderstood because of the lack of field data on the actualexposure of earthworms to currently used molecules.Alltogether, using earthworm services in cropping systems is

Fig. 4 There are several approaches to increase earthworm beneficialeffects on crops and agroecosystems. The gradient depicted in thisillustration distinguishes systems that function on the basis of self-

organization from systems that rely on human intervention to achievetheir ecological functions. Modified from Blouin et al. 2013

Earthworm services for cropping systems 563

very likely to contribute increasing agricultural sustainability.Nevertheless, additional long-term field studies will be essen-tial to fully understand the impact of earthworms on cropproduction. In particular, these studies should strive to (i)disentangle the mechanisms through which earthworms im-pact fertility and plant growth and (ii) assess the relativeinfluence of agricultural practices on earthworm populations

References

Appelhof M, Fenton MF, Harris BL (1993) Worms eat our garbage.Classroom activities for a better environment. Flower Press,Kalamazoo, p 214

Arancon NQ, Edwards CA (2011) The use of vermicomposts as soilamendments for production of field crops. In: Edwards CA,Arancon NQ, Sherman R (eds) Vermiculture technology: earth-worms, organic wastes, and environmental management. CRCPress, Boca Raton, pp 129–151

Atiyeh RM, Dominguez J, Subler S, Edwards CA (2000) Changes inbiochemical properties of cow manure during processing by earth-worms (Eisenia andrei, Bouche) and the effects on seedling growth.Pedobiologia 44:709–724. doi:10.1078/S0031-4056(04)70084-0

Baker GH, Carter PJ, Barrett VJ (1999) Influence of earthworms,Aporrectodea spp. (Lumbricidae), on pasture production in south-eastern Australia. Aust J Agric Res 50:1247–1257. doi:10.1071/AR98182

Bauer C, Römbke J (1997) Factors influencing the toxicity of twopesticides on three lumbricid species in laboratory tests. Soil BiolBiochem 29:705–708. doi:10.1016/S0038-0717(96)00198-8

Birkas M, Jolankai M, Gyuricza C, Percze A (2004) Tillage effectson compaction, earthworms and other soil quality indicators inHungary. Soil Tillage Res 78:185–196. doi:10.1016/j.still.2004.02.006

Blackwell PS (2000) Management of water repellency in Australia,and risks associated with preferential flow, pesticide concentra-tion and leaching. J Hydrol 231(232):384–395. doi:10.1016/S0022-1694(00)00210-9

Blanchart E, Lavelle P, Braudeau E, Le Bissonnais Y, Valentin C (1997)Regulation of soil structure by geophagous earthworm activities inhumid savannas of Côte d’Ivoire. Soil Biol Biochem 29:431–439.doi:10.1016/S0038-0717(96)00042-9

Blanchart E, Albrecht A, Alegre J, Duboisset A, Gilot C, Pashanasi B,Lavelle P, Brussaard L (1999) Effects of earthworms on soil struc-ture and physical properties. In: Lavelle P, Brussaard L, Hendrix P(eds) Earthworm management in tropical agroecosystems. CABInternational, Wallingford, pp 149–172

Blouin M, Zuily-Fodil Y, Pham-Thi AT, Laffray D, Reversat G, Pando A,Tondoh J, Lavelle P (2005) Belowground organism activities affectplant aboveground phenotype, inducing plant tolerance to parasites.Ecol Lett 8:202–208. doi:10.1111/j.1461-0248.2004.00711.x

Blouin M, Lavelle P, Laffray D (2007) Drought stress in rice (Oryzasativa L.) is enhanced in the presence of the compacting earthwormMillsonia anomala. Environ Exp Bot 60:352–359. doi:10.1016/j.envexpbot.2006.12.017

Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR,Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ(2013) A review of earthworm impact on soil function and ecosys-tem services. Eur J Soil Sci 64:161–182. doi:10.1111/ejss.12025

Bohlen PJ, Parmelee RW, McCartney DA, Ewards CA (1997)Earthworm effects on carbon and nitrogen dynamics of surface litter

in corn agroecosystems. Ecol Appl 7:1341–1349. doi:10.1890/1051-0761(1997)007[1341:EEOCAN]2.0.CO;2

Bossuyt H, Six J, Hendrix PF (2005) Protection of soil carbon bymicroaggregates within earthworm casts. Soil Biol Biochem 37:251–258. doi:10.1016/j.soilbio.2004.07.035

Boström U (1995) Earthworm populations (Lumbricidae) in ploughedand undisturbed leys. Soil Tillage Res 35:125–133. doi:10.1016/0167-1987(95)00489-0

Bouché M.B., (1972) Lombriciens de France. Ecologie et systematique,INRA, Ann. Zool. Anim. Publication, Paris, 671 pp

Bouché M, Al-Addan F (1997) Role of earthworms in the N cycle: afalsifiable assessment. Soil Biol Biochem 29:375–380. doi:10.1016/S0038-0717(96)00045-4

Briones MJI, Bol R (2003) Natural abundance of C-13 and N-15 inearthworms from different cropping treatments. Pedobiologia 47:560–567. doi:10.1016/S0031-4056(04)70238-3

Brown GG (1995) How do earthworms affect microfloral and faunalcommunity diversity? Plant Soil 170:209–231. doi:10.1007/BF02183068

Brown GG, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S,Barois I, Lavelle P, Blanchart E, Blakemore RJ, Spain AV, Boyer J(1999) Effects of earthworms on plant production in the tropics. In:Lavelle P, Brussaard L, Hendrix P (eds) The management of earth-worms in tropical agroecosystems. CAB International, Wallingford,pp 87–148

Brown GG, Edwards CA, Brussaard L (2004) How earthworms affectplant growth: burrowing into the mechanisms. In: Edwards CA (ed)Earthworm ecology. CRC Press, Boca Raton, pp 13–49

Brussaard L, de Ruiter PC, Brown GG (2007) Soil biodiversity foragricultural sustainability. Agric Ecosyst Environ 121:233–244.doi:10.1016/j.agee.2006.12.013

Burtelow AE, Bohlen PJ, Groffman PM (1998) Influence of exoticearthworm invasion on soil organic matter, microbial biomassand denitrification potential in forest soils of the northeastUnited States. Appl Soil Ecol 9:197–202. doi:10.1016/S0929-1393(98)00075-4

Butt KR, Frederickson J, Morris RM (1997) The earthworm inoculationunit technique: an integrated system for cultivation and soil-inoculation of earthworms. Soil Biol Biochem 29:251–257. doi:10.1016/S0038-0717(96)00053-3

Canellas LP, Olivares FL, Okorokova-Facanha AL, Facanha AR (2002)Humic acids isolated from earthworm compost enhance root elon-gation, lateral root emergence, and plasma membrane H+−ATPaseactivity in maize roots. Plant Physiol 130:1951–1957. doi:10.1104/pp. 007088

Capowiez Y, Cadoux S, Bouchant P, Ruy S, Roger-Estrade J, Richard G,Boizard H (2009) The effect of tillage type and cropping system onearthworm communities, macroporosity and water infiltration. SoilTillage Res 105:209–216. doi:10.1016/j.still.2009.09.002

Carpenter D, HodsonM E, Eggleton P, Kirk C (2007) Earthworm inducedmineral weathering: preliminary results. Eur J Soil Biol 43:S176–S183. doi:10.1016/j.ejsobi.2007.08.053

Chan KY (2001) An overview of some tillage impacts on earthwormpopulation abundance and diversity - implications for functioning insoils. Soil Tillage Res 57:179–191. doi:10.1016/S0167-1987(00)00173-2

Chan KY, Baker GH, Conyers MK, Scott B, Munro K (2004)Complementary ability of three European earthworms (Lumbricidae)to bury lime and increase pasture production in acidic soils of south-eastern Australia. Appl Soil Ecol 26:257–271. doi:10.1016/j.apsoil.2003.12.004

Chauvel A, GrimaldiM, Barros E, Blanchart E, Desjardins T, SarrazinM,Lavelle P (1999) Pasture damage by an Amazonian earthworm.Nature 398:32–33. doi:10.1038/17946

Choo L, Baker H (1998) Influence of four commonly used pesticides on thesurvival, growth, and reproduction of the earthworm Apporectodea

564 M. Bertrand et al.

trapezoides (Lumbricidae). Aust J Agric Res 49:1297–1303. doi:10.1071/A98021

Clements RO, Murray PJ, Sturdy RG (1991) The impact of 20 yearsabsence of earthworms and 3 levels of N-fertilizer on a grasslandsoil. Agric Ecosyst Environ 36:75–85. doi:10.1016/0167-8809(91)90037-X

Cluzeau D, Binet F, Vertes F, Simon JC, Riviere JM, Trehen P (1992)Effects of intensive cattle trampling on soil plant earthworms systemin 2 grassland types. Soil Biol Biochem 24:1661–1665. doi:10.1016/0038-0717(92)90166-U

Costello DM, Lamberti GA (2009) Biological and physical effects ofnon-native earthworms on nitrogen cycling in riparian soils. SoilBiol Biochem 41:2230–2235. doi:10.1016/j.soilbio.2009.08.007

Cuendet G (1983) Predation on earthworms by the black-headed gull(Larusridibundus L.). In: Satchell JE (ed) Earthworm ecology – fromDarwin to Vermiculture. Chapman & Hall, London, pp 415–424

Curry JP (2004) Factors affecting the abundance of earthworms in soils.In: Edwards CA (ed) Earthworm ecology. CRC, Boca Raton, pp115–188

Darwin C (1881) The formation of vegetable mould through the action ofworms, with observations on their habits. John Murray, London

De Oliveira T, Bertrand M, Roger-Estrade J (2012) Short-term effects ofploughing on the abundance and dynamics of two endogeic earth-worm species in organic cropping systems in northern France. SoilTillage Res 119:76–84. doi:10.1016/j.still.2011.12.008

Decaëns T, Mariani L, Betancourt N, Jiménez JJ (2003) Seed dispersionby surface casting activities of earthworms in Colombian grasslands.Acta Oecol 24:175–185. doi:10.1016/S1146-609X(03)00083-3

Domínguez J, Bohlen PJ, Parmelee RW (2004) Earthworms increasenitrogen leaching to greater soil depths in row crop agroecosystems.Ecosytems 7:672–685. doi:10.1007/s10021-004-0150-7

Don A, Steinberg B, Schöning I, Pritsch K, Joschko M, Gleixner G,Schulze E-D (2008) Organic carbon sequestration in earthwormburrows. Soil Biol Biochem 40:1803–1812. doi:10.1016/j.soilbio.2008.03.003

Doube BM, Ryder MH, Davoren CW, Stephens PM (1994) Enhancedroot nodulation of subterranean clover (Trifolium subterraneum) byRhizobium leguminosarium biovartrifolii in the presence of theearthworm Aporrectodea trapezoides (Lumbricidae). Biol FertilSoils 18:169–174. doi:10.1007/BF00647663

Edwards CA (2004) Earthworm ecology. CRC Press, Boca RatonEdwards CA, Bohlen PJ, (1996) Ed., Biology and ecology of earth-

worms. Chapman & Hall, London, 426 pEdwards CA, Arancon NQ, Sherman R (2011) Vermiculture technology:

earthworms, organic wastes, and environmental management. CRCPress, Boca Raton, p 601

Ehlers W (1975) Observations on earthworm channels and infiltration ontilled and untilled loess soil. Soil Sci 119:242–249. doi:10.1097/00010694-197503000-00010

Eijsackers H, Beneke P, Maboeta M, Louw JPE, Reinecke AJ (2005) Theimplications of copper fungicide usage in vineyards for earthwormactivity and resulting sustainable soil quality. Ecotoxicol EnvironSaf 62:99–111. doi:10.1016/j.ecoenv.2005.02.017

Eisenhauer N, Scheu S (2008) Earthworms as drivers of the competitionbetween grasses and legumes. Soil Biol Biochem 40:2650–2659.doi:10.1016/j.soilbio.2008.07.010

Eisenhauer N, Schuy M, Butenschoen O, Scheu S (2009) Direct andindirect effects of endogeic earthworms on plant seeds. Pedobiologia52:151–162. doi:10.1016/j.pedobi.2008.07.002

Eriksen-Hamel NS, Whalen JK (2007) Impacts of earthworms on soilnutrients and plant growth in soybean and maize agroecosystems.Agric Ecosyst Environ 120:442–448. doi:10.1016/j.agee.2006.11.004

Ernst G, Felten D, Volhand M, Emmerling C (2008) Impact of ecologi-cally different earthworm species on soil water characteristics. Eur JSoil Biol 45:207–213. doi:10.1016/j.ejsobi.2009.01.001

Evans AC, Guild WJM (1948) Studies on the relationships betweenearthworms and soil fertility; chapter V. Field population. ApplBiol 35:485–493

Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007)Stability of organic carbon in deep soil layers controlled by freshcarbon supply. Nature 450:277–281. doi:10.1038/nature06275

Gange AC (1993) Translocation of mycorrhizal fungi by earthwormsduring early succession. Soil Biol Biochem 25:1021–1026. doi:10.1016/0038-0717(93)90149-6

Gerard BM, Hay RKM (1979) The effect on earthworms ofploughing, tined cultivation, direct drilling and nitrogen in abarley monoculture system. J Agric Sci 93:147–155. doi:10.1017/S0021859600086238

Giri S (1995) Short term input operational experiment in tea garden withapplication of organic matter and earthworms. M. Phil. Thesis,Sambalpur University Sambalpur, India

Grdiša M, Gršić K, Grdiša MD (2013) Earthworms – role in soil fertilityto the use in medicine and as a food. Invertebr Surviv J 10:38–45

Groffman PM, Bohlen PJ, Fisk MC, Fahey TJ (2004) Exotic earthworminvasion and microbial biomass in temperate forest soils.Ecosystems 7:45–54. doi:10.1007/s10021-003-0129-9

Hale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effectson hardwood forest floor, nutrient availability and native plants: amesocosm study. Oecologia 155:509–518. doi:10.1007/s00442-007-0925-6

Hallaire V, Curmi P, Duboisset A, Lavelle P, Pashanasi B (2000) Soilstructure changes induced by the tropical earthworm Pontoscolexcorethrurus and organic inputs in a Peruvian ultisol. Eur J Soil Biol36:35–44. doi:10.1016/S1164-5563(00)01048-7

Hendrix PF, Peterson AC, Beare MH, Coleman DC (1998) Long-termeffects of earthworms on microbial biomass nitrogen in coarse andfine textured soils. Appl Soil Ecol 9:375–380. doi:10.1016/S0929-1393(98)00092-4

Horn MA, Mertel R, Gehre M, Kästner M, Drake HL (2006) In vivoemission of dinitrogen by earthworms via denitrifying bacteria in thegut. Appl EnvironMicrobiol 72:1013–1018. doi:10.1128/AEM. 72.2.1013-1018.2006

House GJ, Parmelee RW (1985) Comparison of soil arthropods andearthworms from conventional and no-tillage agroecosystems. SoilTillage Res 5:351–360. doi:10.1016/S0167-1987(85)80003-9

Ivask M, Kuu A, Sizov E (2007) Abundance of earthworm species inEstonian arable soils. Eur J Soil Biol 43:S39–S42. doi:10.1016/j.ejsobi.2007.08.006

Jarvis N, Etana A, Stagnitti F (2007) Water repellency, near-saturatedinfiltration and preferential solute transport in a macroporous claysoil. Geoderma 143:223–230. doi:10.1016/j.geoderma.2007.11.015

Jegou D, Brunotte J, Rogasik H, Capowiez Y, Diestel H, Schrader S,Cluzeau D (2002) Impact of soil compaction on earthworm burrowsystems using X-ray computed tomography: preliminary study. EurJ Soil Biol 38:329–336. doi:10.1016/S1164-5563(02)01148-2

Jouquet P, Podwojewski P, Bottinelli N, Mathieu J, Ricoy M, Orange D,Duc TT, Valentin C (2007) Above-ground earthworm casts affectwater runoff and soil erosion in Northern Vietnam. Catena 74:13–21. doi:10.1016/j.catena.2007.12.006

Kladivko EJ (2001) Tillage systems and soil ecology. Soil Tillage Res 61:61–76. doi:10.1016/S0167-1987(01)00179-9

Lachnicht SL, Parmelee RW, Mccartney D, Allen M (1997)Characteristics of macroporosity in a reduced tillage agroecosystemwith manipulated earthworm populations: Implications for infiltra-tion and nutrient transport. Soil Biol Biochem 29:493–498. doi:10.1016/S0038-0717(96)00106-X

Lal R (2004) Soil carbon sequestration impacts on global climate changeand food security. Science 304:1623–1627. doi:10.1126/science.1097396

Laossi K-R, Noguera DC, Bartolomé-Lasa A, Mathieu J, Blouin M,Barot S (2009) Effects of endogeic and anecic earthworms on the

Earthworm services for cropping systems 565

competition between four annual plants and their relative reproduc-tion potential. Soil Biol Biochem 41:1668–1673. doi:10.1016/j.soilbio.2009.05.009

Laossi K.-R, Decaëns T, Jouquet P, Barot S (2010a). Can we predict howearthworm effects on plant growth vary with soil properties?Applied and Environmental Soil Science, Article ID 784342: 6.DOI: 10.1155/2010/784342

Laossi K-R, Noguera D-C, Barot S (2010b) Earthworm-mediated mater-nal effects on seed germination and seedling growth in three annualplants. Soil Biol Biochem 42:319–323. doi:10.1016/j.soilbio.2009.11.010

Larink O, Schrader S (2000) Rehabilitation of degraded compacted soilby earthworms, in Subsoil Compaction. Adv GeoEcol 32:284–294

Lavelle P, Martin A (1992) Small-scale and large-scale effects ofendogeic earthworms on soil organic matter dynamics in soils ofthe humid tropics. Soil Biol Biochem 24:1491–1498. doi:10.1016/0038-0717(92)90138-N

Lavelle P, Spain AV (2001) Soil ecology. Kluwer Scientific Publications,Amsterdam

Lavelle P, Melendez G, Pashanasi B, Schaefer R (1992) Nitrogen miner-alization and reorganization in casts of the geophagous tropicalearthworm Pontoscolex corethrurus (Glossoscolecidae). Biol FertilSoils 14:49–53. doi:10.1007/BF00336302

Lavelle P, Barois I, Blanchart E, Brown G, Decaëns T, Fragoso C,Jimenez JJ, Kajondo KK, Moreno A, Pashanasi B, Senapati B,Villenave C (2001) Earthworms as a resource in tropicalagroecosystems. In: SubbaRao NS, Dommergues YR (eds)Microbial interactions in agriculture and forestry. Science Publishers,Inc., Enfield, pp 163–181

Le Bayon RC, Moreau S, Gascuel-Odoux C, Binet F (2002) Annualvariations in earthworm surface-casting activity and soil transport bywater runoff under a temperate maize agroecosytem. Geoderma 106:121–135. doi:10.1016/S0016-7061(01)00121-5

Lee KE (1985) Ed.. Earthworms – Their ecology and relationships withsoils and land use. Academic press, Australia, 411 p

Leroy BLM, Schmidt O, Van den Bossche A, Reheul D,MoensM (2008)Earthworm population dynamics as influenced by the quality ofexogenous organic matter. Pedobiologia 52:139–150. doi:10.1016/j.pedobi.2008.07.001

Li X, Fisk MC, Fahey TJ, Bohlen PJ (2002) Influence of earthworminvasion on soil microbial biomass and activity in a northern hard-wood forest. Soil Biol Biochem 34:1929–1937. doi:10.1016/S0038-0717(02)00210-9

Loeuille N, Barot S, Georgelin E, Kylafis G, Lavigne C (2013) Eco-evolutionary dynamics of agricultural networks: implications for asustainable management. Adv Ecol Res 49:339–435. doi:10.1016/B978-0-12-420002-9.00006-8

Low AJ (1972) The effect of cultivation on the structure and otherphysical characteristics of grassland and arable soils (1945–1970).J Soil Sci 23:363–380. doi:10.1111/j.1365-2389.1972.tb01668.x

Lubbers IM, Groenigen KV, Fonte SJ, Six J, Brussaard L, Groenigen JW(2013) Greenhouse-gas emissions from soils increased by earth-worms. Nature Climate Change. doi:10.1038/nclimate1692

Malezieux E (2012) Designing cropping systems from nature. AgronSustain Dev 32:15–29. doi:10.1007/s13593-011-0027-z

Marinissen JCY, de Ruiter PC (1993) Contribution of earthworms tocarbon and nitrogen cycling in agro-systems. Agric EcosystEnviron 47:59–74. doi:10.1016/0167-8809(93)90136-D

Martin GA, Stockdill SMJ (1976) Machine speeds job of earthwormintroduction. N Z J Agric 132:6–7

McLean MA, Parkinson D (2000) Field evidence of the effects of theepigeic earthwormDendrobaena octaedra on the microfungal com-munity in pine forest floor. Soil Biol Biochem 32:351–360. doi:10.1016/S0038-0717(99)00161-3

Menezes-Oliveira VB, Scott-Fordsmand JJ, Rocco A, Soares AM,Amorim MJ (2011) Interaction between density and Cu toxicity

for Enchytraeus crypticus and Eisenia fetida reflecting fieldscenarios. Sci Total Environ 409:3370–3374. doi:10.1016/j.scitotenv.2011.04.033

Mohasin M, Bhowmik P, Banerjee A, Somchoudhury A (2005) Effect ofsome herbicides on earthworm (Metaphireposthuma) under fieldconditions. J Crop Weed 1:17–19

Mouquet N, Loreau M (2003) Community patterns in source-sinkmetacommunities. Am Nat 162:544–557. doi:10.1086/378857

Muscolo A, Cutrupi S, Nardi S (1998) IAA detection in humic sub-stances. Soil Biol Biochem 30:1199–1201. doi:10.1016/S0038-0717(98)00005-4

Noguera D, Laossi K-R, Lavelle P, Cruz de Carvalho M-H, Asakawa N,Botero C, Barot S (2011) Amplifying the benefits of agroecology byusing the right cultivars. Ecol Appl 21:2349–2356. doi:10.1890/10-2204.1

Nuutinen V (1992) Earthworm community response to tillage and residuemanagement on different soil types in southern Finland. Soil TillageRes 23:221–239. doi:10.1016/0167-1987(92)90102-H

Olele NF, Okonkwo JC (2012) Replacement of fish meal with gradedlevels of earthwormmeal in the diet of fingerlings: effect on feed andgrowth parameters. J Agric Sci Technol A 2:901–908

Paoletti M, Buscardo E, VanderJagt D, Pastuszyn A, Pizzoferrato L,Huang Y, Chuang L, Millson M, Cerda H, Torres F, Glew R(2003) Nutrient content of earthworms consumed by Ye’KuanaAmerindians of the Alto Orinoco of Venezuela. Proc R Soc B BiolSci 270:249–257. doi:10.1098/rspb.2002.2141

Peigné J, Ball BC, Roger-Estrade J, David C (2007) Is conservationtillage suitable for organic farming? A review. Soil Use Manag 23:129–144. doi:10.1111/j.1475-2743.2006.00082.x

Peigne J, Cannavaciuolo M, Gautronneau Y, Aveline A, Giteau JL,Cluzeau D (2009) Earthworm populations under different tillagesystems in organic farming. Soil Tillage Res 104:207–214. doi:10.1016/j.still.2009.02.011

Pelosi C, Bertrand M, Roger-Estrade J (2009) Earthworm community inconventional, organic and direct seeding with living mulch croppingsystems. Agron Sustain Dev 29:287–295. doi:10.1051/agro/2008069

Pelosi C, Barot S, Capowiez Y, Hedde M, Vandenbulcke F (2014)Pesticides and earthworms. A review. Agron Sustain Dev 34:199–228. doi:10.1007/s13593-013-0151-z

Pitkänen J, Nuutinen V (1998) Earthworm contribution to infiltration andsurface runoff after 15 years of different soil management. Appl SoilEcol 9:411–415. doi:10.1016/S0929-1393(98)00098-5

Puga-Freitas R, Barot S, Taconnat L, Renou J-P, BlouinM (2012a) Signalmolecules mediate the impact of the earthworm Aporrectodeacaliginosa on growth, development and defence of the plantArabidopsis thaliana. PLoS ONE 7:e49504. doi:10.1371/journal.pone.0049504

Puga-Freitas R, Abbad S, Gigon A, Garnier-Zarli E, Blouin M(2012b) Control of cultivable IAA-producing bacteria by theplant Arabidopsis thaliana and the earthworm Aporrectodeacaliginosa. Appl Environ Soil Sci 2012, 307415. doi:10.1155/2012/307415

Pulleman MM, Six J, Uyl A, Marinissen JCY, Jongmans AG (2005)Earthworms and management affect organic matter incorporationand microaggregate formation in agriculture soils. Appl Soil Ecol29:1–15. doi:10.1016/j.apsoil.2004.10.003

Reddell P, Spain AV (1991) Transmission of infective Frankia(Actinomycetales) propagules in casts of the endogeic earthwormPontoscolex corethrurus (Oligocheta: Glossoscolecidae). Soil BiolBiochem 23:767–774. doi:10.1016/0038-0717(91)90148-D

Riley H, Pommeresche R, Eltun R, Hansen S, Korsaeth A (2008) Soilstructure, organic matter and earthworm activity in a comparison ofcropping systems with contrasting tillage, rotations, fertilizer levelsand manure use. Agric Ecosyst Environ 124:275–284. doi:10.1016/j.agee.2007.11.002

566 M. Bertrand et al.

Ritsema CJ, Dekker LW (2000) Preferential flow in water repellent sandysoils: principles andmodeling implications. J Hydrol 231(232):308–319. doi:10.1016/S0022-1694(00)00203-1

Roger-Estrade J, Anger C, BertrandM, Richard G (2010) Tillage and soilecology: partners for sustainable agriculture. Soil Tillage Res 111:33–40. doi:10.1016/j.still.2010.08.010

Rosas-MedinaMA, de Leon-Gonzalez F, Flores-Macias A, Payan-ZelayaF, Borderas-Tordesillas F, Gutierrez-Rodriguez F, Fragoso-GonzalezC (2010) Effect of tillage, sampling date and soil depth on earth-worm population on maize monoculture with continuous stoverrestitutions. Soil Tillage Res 108:37–42. doi:10.1016/j.still.2010.03.008

Sander T, Gerke HH, Rogasik H (2008) Assessment of Chinese paddy-soil structure using X-ray computed tomography. Geoderma 145:303–314. doi:10.1016/j.geoderma.2008.03.024

Scheu S (2003) Effects of earthworms on plant growth: patterns andperspectives. Pedobiologia 47:846–856. doi:10.1078/0031-4056-00270

Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivoreand the herbivore system: effects of earthworms and Collembola onplant growth and aphid development. Oecologia 119:541–551. doi:10.1007/s004420050817

Scheu S, Schlitt N, Tunov AV, Newington JE, Jones TH (2002) Effects ofthe presence and community composition of earthwoms on micro-bial community functioning. Oecologia 133:254–260. doi:10.1007/s00442-002-1023-4

Scown J, Baker G (2006) The influence of livestock dung on the abun-dance of exotic and native earthworms in a grassland in south-eastern Australia. Eur J Soil Biol 42:310–315. doi:10.1016/j.ejsobi.2006.07.036

Shen Y (2010) Earthworms in traditional Chines medicine (Oligocaea:Lumbricidae, Megascolecidae). Zool Middle East, Suppl 2:171–173. doi:10.1080/09397140.2010.10638470

Shuster WD, McDonald LP, McCartney DA, Parmelee RW, Studer NS,Stinner BR (2002) Nitrogen source and earthworm abundance af-fected runoff volume and nutrient loss in a tilled-cornagroecosystem. Biol Fertil Soils 35:320–327. doi:10.1007/s00374-002-0474-4

Stephens PM, Davoren CW (1997) Influence of the earthwormsAporrectodea trapezoides and A. rosea on the disease severity ofRhizoctonia solani on subterranean clover and ryegrass. Soil BiolBiochem 29:511–516. doi:10.1016/S0038-0717(96)00108-3

Stephens PM, Davoren CW, Doube BM, RyderMH (1994) Ability of thelumbricid earthworms Aporrectodea rosea and Aporrectodeatrapezoides to reduce the severity of take-all under greenhouse andfield conditions. Soil Biol Biochem 26:1291–1297. doi:10.1016/0038-0717(94)90209-7

Stockdill SMJ (1959) Earthworms improve pasture growth. N Z J Agric98:227–233

Stockdill SMJ (1966) The effect of earthworms on pastures. Proc N ZProc NZ Ecol Soc 13:68–75

Stockdill S (1982) Effects of introduced earthworms on the productivityof New Zealand pastures. Pedobiologia 24:29–35

Svendsen TS, Hansen PE, Sommer C, Martinussen T, Gronvold J, HolterP (2005) Life history characteristics of Lumbricus terrestris andeffects of the veterinary antiparasitic compounds ivermectin andfenbendazole. Soil Biol Biochem 37:927–936. doi:10.1016/j.soilbio.2004.10.014

Tiroesele B, Moreki JC (2012) Termites and earthworms as potentialalternative sources of protein for poultry. Int J Agro Vet Med Sci6:368–376

Tomlin AD, Miller JJ (1988) Impact of ring-billed gull (Larusdelawarensis ord.) foraging on earthworm populations of south-western Ontario agricultural soils. Agric Ecosyst Environ 20:165–173. doi:10.1016/0167-8809(88)90108-9

Valckx J, Pennings A, Leroy T, Berckmans D, Govers G, Hermy M,Muys B (2010) Automated observation and analysis of earthwormsurface behaviour under experimental habitat quality and availabil-ity conditions. Pedobiologia 53:259–263. doi:10.1016/j.pedobi.2009.12.005

Winding A, Rønn R, Hendriksen NB (1997) Bacteria and protozoa in soilmicrohabitats as affected by earthworms. Biol Fertil Soils 24:133–140. doi:10.1007/s003740050221

Wyss E, Glasstetter M (1992) Tillage treatments and earthworm distribu-tion in a swiss experimental corn field. Soil Biol Biochem 24:1635–1639. doi:10.1016/0038-0717(92)90162-Q

Earthworm services for cropping systems 567